Molecular mechanisms of TGFβ receptor-triggered signaling cascades rapidly induced by the calcineurin inhibitors cyclosporin A and FK506

Journal of Immunology

Volumn 181, Issue 4, 2008, Pages 2831-2845

  Akool, El Sayed ^a   Doller, Anke ^a   Babelova, Andrea ^a   Tsalastra, Wasiliki ^a   Moreth, Kristin ^a   Schaefer, Liliana ^a   Pfeilschifter, Josef ^a   Eberhardt, Wolfgang ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ACETYLCYSTEINE; CONNECTIVE TISSUE GROWTH FACTOR; CYCLOSPORIN A; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE; SMAD PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; TACROLIMUS; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; CALCINEURIN; CYCLOSPORIN; MADH2 PROTEIN, RAT; PROTEIN SERINE THREONINE KINASE; TGF BETA TYPE I RECEPTOR; TGF-BETA TYPE I RECEPTOR; TGFB1 PROTEIN, RAT; TRANSFORMING GROWTH FACTOR BETA TYPE II RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR-BETA TYPE II RECEPTOR;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MALE; MESANGIUM CELL; NEPHROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN SYNTHESIS; RAT; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; ANIMAL; BIOSYNTHESIS; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; FIBROSIS; HUMAN; IMMUNOLOGY; INTRAPERITONEAL DRUG ADMINISTRATION; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; WISTAR RAT;

ANIMALS; CALCINEURIN; CELLS, CULTURED; CYCLOSPORINE; FIBROSIS; HUMANS; INJECTIONS, INTRAPERITONEAL; MALE; MESANGIAL CELLS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, WISTAR; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; TACROLIMUS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 53149099360     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.4.2831     Document Type: Article

References (52)

1. Schreiber, S. L., and G. R. Crabtree. 1992. The mechanism of action of cyclosporine A and FK506. Immunol. Today 13: 136-142.
2. Mihatsch, M. J., M. Kyo, K. Morozumi, Y. Yamaguchi, V. Nickeleit, and B. Ryffel. 1998. The side-effects of ciclosporine-A and tacrolimus. Clin. Nephrol. 49: 356-363.
3. Fellstrom, B. 2004. Cyclosporine nephrotoxicity. Transplant. Proc. 36: S220-S223.
4. Duymelinck, C., J. T. Deng, S. E. Dauwe, M. E. De Broe, and G. A. Verpooten. 1998. Inhibition of the matrix metalloproteinase system in a rat model of chronic cyclosporine nephropathy. Kidney Int. 54: 804-818.
5. Woessner, J. F., Jr. 1991. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J. 5: 2145-2154.
6. Eddy, A. A. 2000. Molecular basis of renal fibrosis. Pediatr. Nephrol. 15: 290-301.
7. Gore-Hyer, E., D. Shegogue, M. Markiewicz, S. Lo, D. Hazen-Martin, E. L. Greene, G. Grotendorst, and M. Trojanowska. 2002. TGFβ and CTGF have overlapping and distinct fibrogenic effects on human renal cells. Am. J. Physiol. 283: F707-F716.
8. Okada, H., T. Kikuta, T. Kobayashi, T. Inoue, Y. Kanno, M. Takigawa, T. Sugaya, J. B. Kopp, and H. Suzuki. 2005. Connective tissue growth factor expressed in tubular epithelium plays a pivotal role in renal fibrogenesis. J. Am. Soc. Nephrol. 16: 133-143.
9. Khanna, A. K., V. R. Cairns, C. G. Becker, and J. D. Hosenpud. 1999. Transforming growth factor (TGF)-βmimics and anti-TGF-β antibody abrogates the in vivo effects of cyclosporine: demonstration of a direct role of TGF-β in immunosuppression and nephrotoxicity of cyclosporine. Transplantation 67: 882-889.
10. Ziyadeh, F. N., B. B. Hoffman, D. C. Han, M. C. Iglesias-De La Cruz, S. W. Hong, M. Isono, S. Chen, T. A. McGowan, and K. Sharma. 2000. Longterm prevention of renal insufficiency, excess matrix gene expression, and glomerular mesangial matrix expansion by treatment with monoclonal antitransforming growth factor-β antibody in db/db diabetic mice. Proc. Natl. Acad. Sci. USA 97: 8015-8020.
11. Islam, M., J. F. Burke, Jr., T. A. McGowan, Y. Zhu, S. R. Dunn, P. McCue, J. Kanalas, and K. Sharma. 2001. Effect of anti-transforming growth factor-β antibodies in cyclosporine-induced renal dysfunction. Kidney Int. 59: 498-506.
12. Ling, H., X. Li, S. Jha, W. Wang, L. Karetskaya, B. Pratt, and S. Ledbetter. 2003. Therapeutic role of TGF-β-neutralizing antibody in mouse cyclosporine A nephropathy: morphologic improvement associated with functional preservation. J. Am. Soc. Nephrol. 14: 377-388.
13. Fukasawa, H., T. Yamamoto, H. Suzuki, A. Togawa, N. Ohashi, Y. Fujigaki, C. Uchida, M. Aoki, M. Hosono, M. Kitagawa, and A. Hishida. 2004. Treatment with anti-TGF-βantibody ameliorates chronic progressive nephritis by inhibiting Smad/TGF-β signaling. Kidney Int. 65: 63-74.
14. Massague, J. 1998. TGF-βsignal transduction Annu. Rev. Biochem. 67: 753-791.
15. Piek, E., C. H. Heldin, and P. Ten Dijke. 1999. Specificity, diversity, and regulation in TGF-β superfamily signaling. FASEB J. 13: 2105-2124.
16. Miyazono, K., P. ten Dijke, and C. H. Heldin. 2000. TGF-β signaling by Smad proteins. Adv. Immunol. 75: 115-157.
17. Chen, Y., I. E. Blom, S. Sa, R. Goldschmeding, D. J. Abraham, and A. Leask. 2002. CTGF expression in mesangial cells: involvement of SMADs, MAP kinase, and PKC. Kidney Int. 62: 1149-1159.
18. Marti, H. P., L. Lee, M. Kashgarian, and D. H. Lovett. 1994. Transforming growth factor-beta 1 stimulates glomerular mesangial cell synthesis of the 72-kd type IV collagenase. Am. J. Pathol. 144: 82-94.
19. Akool, E. S., A. Doller, R. Muller, P. Gutwein, C. Xin, A. Huwiler, J. Pfeilschifter, and W. Eberhardt. 2005. Nitric oxide induces TIMP-1 expression by activating the transforming growth factor β-Smad signaling pathway. J. Biol. Chem. 280: 39403-39416.
20. Pfeilschifter, J., and K. Vosbeck. 1991. Transforming growth factor beta 2 inhibits interleukin 1 beta- and tumour necrosis factor alpha-induction of nitric oxide synthase in rat renal mesangial cells. Biochem. Biophys. Res. Commun. 175: 372-379.
21. Zawel, L., J. L. Dai, P. Buckhaults, S. Zhou, K. W. Kinzler, B. Vogelstein, and S. E. Kern. 1998. Human Smad3 and Smad 4 are sequence-specific transcription activators. Mol. Cell 1: 611-617.
22. Eberhardt, W., M. Schulze, C. Engels, E. Klasmeier, and J. Pfeilschifter. 2002. Glucocorticoid-mediated suppression of cytokine-induced matrix metalloproteinase-9 expression in rat mesangial cells: involvement of nuclear factor-κB and Ets transcription factors. Mol. Endocrinol. 16: 1752-1766.
23. Xin, C., S. Ren, B. Kleuser, S. Shabahang, W. Eberhardt, H. Radeke, M. Schafer-Korting, J. Pfeilschifter, and A. Huwiler. 2004. Sphingosine 1-phosphate cross-activates the Smad signaling cascade and mimics transforming growth factor-β-induced cell responses. J. Biol. Chem. 279: 35255-35262.
24. Plešková, M., K. F. Beck, M. H. Behrens, A. Huwiler, B. Fichtelscherer, O. Wingerter, R. P. Brandes, A. Mülsch, and J. Pfeilschifter. 2005. Nitric oxide down-regulates the expression of the cytalytic NADPH oxidase subunit Nox 1 in rat renal mesangial cells. FASEB J. 20: 139-141.
25. Sawada, S., G. Suzuki, Y. Kawase, and F. Takaku. 1987. Novel immunosuppressive agent, FK506. In vitro effects on the cloned T cell activation. J. Immunol. 139: 1797-1803.
26. Sawyer, J. S., D. W. Beight, K. S. Britt, B. D. Anderson, R. M. Campbell, T. Goodson, Jr., D. K. Herron, H.Y. Li, W. T. McMillen, N. Mort, et al. 2004. Synthesis and activity of new aryl- and heteroaryl-substituted 5,6-dihydro-4Hpyrrolo[ 1,2-b] pyrazole inhibitors of the transforming growth factor-β type I receptor kinase domain. Bioorg. Med. Chem. Lett. 14: 3581-3584.
27. Krauskopf, A., T. M. Buetler, N. S. D. Nguyen, K. Macé, and U. T. Ruegg. 2002. Cyclosporin A-induced free radical generation is not mediated by cytochrome P-450. Br. J. Pharmacol. 135: 977-986.
28. Moustakas, A., and C. H. Heldin. 2005. Non-Smad TGF-β signals. J. Cell Sci. 118: 3573-3584.
29. Mulder, K. M. 2000. Role of Ras and Mapks in TGFβ signaling. Cytokine Growth Factor Rev. 11: 23-35.
30. Doller, A., E. S. Akool, R. Muller, P. Gutwein, C. Kurowski, J. Pfeilschifter, and W. Eberhardt. 2007. Molecular mechanisms of cyclosporine A inhibition of the cytokine-induced matrix metalloproteinase-9 in glomerular mesangial cells. J. Am. Soc. Nephrol. 18: 581-592.
31. Lin, H. Y., X. F. Wang, E. Ng-Eaton, R. A. Weinberg, and H. F. Lodish. 1992. Expression cloning of the TGF-β type II receptor, a functional transmembrane serine/threonine kinase. Cell 68: 775-785.
32. Bicknell, G. R., S. T. Williams, J. A. Shaw, J. H. Pringle, P. N. Furness, and M. L. Nicholson. 2000. Differential effects of cyclosporine and tacrolimus on the expression of fibrosis-associated genes in isolated glomeruli from renal transplants. Br. J. Surg. 87: 1569-1575.
33. Reynolds, N. J., and W. I. Al-Daraji. 2002. Calcineurin inhibitors and sirolimus: mechanisms of action and applications in dermatology. Clin. Exp. Dermatol. 27: 555-561.
34. Pirsch, J. D., J. Miller, M. H. Deierhoi, F. Vincenti, and R. S. Filo. 1997. A comparison of tacrolimus (FK506) and cyclosporine for immunosuppression after cadaveric renal transplantation: FK506 Kidney Transplant Study Group. Transplantation 63: 977-983.
35. Waiser, J., K. Dell, J. Kreutzkamp, T. Bohler, K. Budde, H. Peters, and H. H. Neumayer. 2006. FK506, transforming growth factor-β1 and mesangial matrix synthesis: parallels and differences compared with cyclosporine A. Cytokine 33: 59-65.
36. Mihatsch, M. J., M. Kyo, K. Morozumi, Y. Yamaguchi, V. Nickeleit, and B. Ryffel. 1998. The side-effects of ciclosporine-A and tacrolimus. Clin. Nephrol. 49: 356-363.
37. Shin, G. T., A. Khanna, R. Ding, V. K. Sharma, M. Lagman, B. Li, and M. Suthanthiran. 1998. In vivo expression of transforming growth factor-β1 in humans: stimulation by cyclosporine. Transplantation 65: 313-318.
38. Pankewycz, O. G., L. Miao, R. Isaacs, J. Guan, T. Pruett, G. Haussmann, and B. C. Sturgill. 1996. Increased renal tubular expression of transforming growth factor βin human allografts correlates with cyclosporine toxicity. Kidney Int. 50: 1634-1640.
39. Wolf, G., E. Mueller, R. A. Stahl, and F. N. Ziyadeh. 1993. Angiotensin IIinduced hypertrophy of cultured murine proximal tubular cells is mediated by endogenous transforming growth factor-β. J. Clin. Invest. 92: 1366-1372.
40. 1 transcription by cyclosporine. FEBS Lett. 358: 109-112.
41. Gao, R., Y. Lu, Y. P. Xin, X. H. Zhang, J. Wang, and Y. P. Li. 2006. The effects of different immunosuppressants on chronic allograft nephropathy by affecting the transforming growth factor-β and Smads signal pathways. Transplant. Proc. 38: 2154-2157.
42. 1 in renal transplant recipients receiving different immunosuppressive regimens. Transplant. Proc. 36: 698-699.
43. 1 in IgA nephropathy. Am. J. Kidney Dis. 38: 1191-1198.
44. 1. J. Leukocyte Biol. 77: 748-758.
45. Annes, J. P., J. S. Munger, and D. B. Rifkin. 2003. Making sense of latent TGFβ activation. J. Cell Sci. 116: 217-224.
46. 1. Mol. Endocrinol. 10: 1077-1083.
47. Jobling, M. F., J. D. Mott, M. T. Finnegan, V. Jurukovski, A. C. Erickson, P. J. Walian, S. E. Taylor, S. Ledbetter, C. M. Lawrence, D. B. Rifkin, and M. H. Barcellos-Hoff. 2006. Isoform-specific activation of latent transforming growth factor β (LTGF-β) by reactive oxygen species. Radiat. Res. 166: 839-848.
48. Krauskopf, A., P. Lhote, O. Petermann, U. T. Ruegg, and T. M. Buetler. 2005. Cyclosporin A generates superoxide in smooth muscle cells. Free Radical Res. 39: 913-919.
49. Tkaczyk, J., and M. Vízek. 2007. Oxidative stress in the lung tissue-sources of reactive oxygen species and antioxidant defence. Prague Med. Rep. 108: 105-114.
50. Hayashida, T., M. Decaestecker, and H. W. Schnaper. 2003. Cross-talk between ERK MAP kinase and Smad signaling pathways enhances TGF-β-dependent responses in human mesangial cells. FASEB J. 17: 1576-1578.
51. Javelaud, D., and A. Mauviel. 2005. Crosstalk mechanisms between the mitogen-activated protein kinase pathways and Smad signaling downstream of TGF-β: implications for carcinogenesis. Oncogene 24: 5742-5750.
52. Yu, L., M. C. Hebert, and Y. E. Zhang. 2002. TGF-β receptor-activated p38 MAP kinase mediates Smad-independent TGF-β responses. EMBO J. 21: 3749 -3759.